A second species of ichthyotoxic Pfiesteria (Dinamoebales, Dinophyceae)

The toxic dinoflagellate Pfiesteria piscicida Steidinger & Burkholder has recently been implicated as the etiologic agent of acute mass mortalities and skin ulcers in menhaden, Brevoortia tyrannus, and other fishes from mid-Atlantic U.S. estuaries. However, evidence for this association is largely circumstantial and controversial. We exposed tilapia (Oreochromis spp.) to Pfiesteria shumwayae Glasgow & Burkholder (identification based on scanning electron microscopy and molecular analyses) and compared the resulting pathology to the so-called Pfiesteria-specific lesions occurring in wild menhaden. The tilapia challenged by high concentrations (2,000-12,000 cells/mL) of P. shumwayaeexhibited loss of mucus coat and scales plus mild petecchial hemorrhage, but no deeply penetrating chronic ulcers like those in wild menhaden. Histologically, fish exhibited epidermal erosion with bacterial colonization but minimal associated inflammation. In moribund fish, loss of epidermis was widespread over large portions of the body. Similar erosion occurred in the mucosa lining the oral and branchial cavities. Gills exhibited epithelial lifting, loss of secondary lamellar structure, and infiltration by lymphoid cells. Epithelial lining of the lateral line canal (LLC) and olfactory organs exhibited severe necrosis. Visceral organs, kidney, and neural tissues (brain, spinal cord, ganglia, peripheral nerves) were histologically normal. An unexpected finding was the numerous P. shumwayae cells adhering to damaged skin, skin folds, scale pockets, LLC, and olfactory tissues. In contrast, histologic evaluation of skin ulcers in over 200 wild menhaden from Virginia and Maryland portions of the Chesapeake Bay and the Pamlico Estuary, North Carolina, revealed that all ulcers harbored a deeply invasive, highly pathogenic fungus now known to be Aphanomyces invadans. In menhaden the infection always elicited severe myonecrosis and intense granulomatous myositis. The consistent occurrence of this fungus and the nature and severity of the resulting inflammatory response indicate that these ulcers are chronic (age >1 week) and of an infectious etiology, not the direct result of an acute toxicosis initiated by Pfiesteria toxin(s) as recently hypothesized. The disease therefore is best called ulcerative mycosis (UM). This study indicates that the pathology of Pfiesteria laboratory exposure is fundamentally different from that of UM in menhaden; however, we cannot rule out Pfiesteria as one of many possible early initiators predisposing wild fishes to fungal infection in some circumstances.

Section: Discussionmentioning

confidence: 99%

Skin ulcers in estuarine fishes: a comparative pathological evaluation of wild and laboratory-exposed fish.

Vogelbein

Shields

Haas

et al. 2001

“…New harmful algae continue to be identified in expanding geographic areas, the most recent being the heterotrophic dinoflagellates Pfiesteria piscicida and P. shumwayae (8,9). These lesion-causing fish killers are reported to produce a narcotizing material that, when airborne, elicits human neurologic impairment and reversible memory deficits (10).…”

mentioning

confidence: 99%

New fish-killing alga in coastal Delaware produces neurotoxins.

Bourdelais

Tomas

Naar

et al. 2002

Ten fish mortality events, involving primarily Atlantic menhaden, occurred from early July through September 2000 in several bays and creeks in Delaware, USA. Two events involved large mortalities estimated at 1-2.5 million fish in Bald Eagle Creek, Rehoboth Bay. Samples from Indian Inlet (Bethany Beach), open to the Atlantic, as well as from an enclosed area of massive fish kills at nearby Bald Eagle Creek and Torque Canal were collected and sent to our laboratory for analysis. Microscopic examination of samples from the fish kill site revealed the presence of a single-cell Raphidophyte alga Chattonella cf. verruculosa at a maximum density of 1.04 x 10(7) cells/L. Naturally occurring brevetoxins were also detected in the bloom samples. Besides the Chattonella species, no other known brevetoxin-producing phytoplankton were present. Chromatographic, immunochemical, and spectroscopic analyses confirmed the presence of brevetoxin PbTx-2, and PbTx-3 and -9 were confirmed by chromatographic and immunochemical analyses. This is the first confirmed report in the United States of brevetoxins associated with an indigenous bloom in temperate Atlantic estuarine waters and of C. cf. verruculosa as a resident toxic organism implicated in fish kills in this area. The bloom of Chattonella continued throughout September and eventually declined in October. By the end of October C. cf. verruculosa was no longer seen, nor was toxin measurable in the surface waters. The results affirm that to avoid deleterious impacts on human and ecosystem health, increased monitoring is needed for brevetoxins and organism(s) producing them, even in areas previously thought to be unaffected.

“…The estuarine dinoflagellates, Pfiesteria piscicida Steidinger & Burkholder and Pfiesteria shumwayae Glasgow & Burkholder, members of the toxic Pfiesteria complex (TPC), have been the primary suspects for causing multiple fish kills in North Carolina and other areas on the east coast of the United States (1)(2)(3)(4). Recent evidence implicated the TPC as a possible human health risk factor.…”

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confidence: 99%

Residential and recreational acquisition of possible estuary-associated syndrome: a new approach to successful diagnosis and treatment.

Shoemaker

2001

Evidence suggests that the estuarine dinoflagellates, Pfiesteria piscicida Steidinger & Burkholder and P. shumwayae Glasgow & Burkholder, members of the toxic Pfiesteria complex (TPC), may release one or more toxins that kill fish and adversely affect human health. In the current study we investigated the potential for undiagnosed cases of possible estuary-associated syndrome (PEAS), as termed by the Centers for Disease Control and Prevention (CDC), in a population that had residential and/or recreational exposure to TPC-affected estuaries, but that did not have direct contact with fish kills or lesioned fish. Age-adjusted visual contrast sensitivity (VCS) was significantly lower and the presence of PEAS-associated symptoms was much higher in the estuary cohort (n = 77) than in combined-control cohorts (n = 87), one without exposure to bodies of water (n = 53) and one with exposure to marine waters (n = 34). In the estuary cohort, 37 individuals met the CDC case definition for PEAS and had significantly lower VCS than non-PEAS cases. The VCS improved and symptoms abated after 2 weeks of treatment with cholestyramine. Cholestyramine, the original drug approved for treatment of hypercholesterolemia, has previously been reported to enhance the elimination rates of a variety of toxins, presumably by interruption of enterohepatic recirculation through toxin entrapment in its polymeric structure and/or anion-exchange process. Control studies showed that repeated VCS testing alone did not improve VCS scores and that cholestyramine treatment did not affect VCS in patients with elevated cholesterol levels. These results suggested that a) susceptible individuals may acquire PEAS through residential and/or recreational contact with TPC-affected estuaries in the absence of an active fish kill; b) VCS is a useful indicator in PEAS diagnosis and treatment monitoring; and c) PEAS can be effectively treated with cholestyramine. Because the study did not use population sampling techniques, the results do not indicate PEAS prevalence. Furthermore, definitive diagnosis of PEAS and association with TPC toxin(s) must await identification of, and a serologic test for, the putative TPC toxin(s).